Abstract

Oxytocin (OT) plays a pivotal role in a variety of complex social behaviors by modulating approach-avoidance motivational tendencies, but recently, its social specificity has been challenged. Here, a randomized, double-blind, placebo-controlled study was conducted with forty young adult men, investigating the effect of a single-dose of OT (24 IU) on behavioral and neural approach-avoidance. Frontal alpha asymmetry, indexing neurophysiological approach-avoidance, was obtained from electroencephalographic recordings while participants were presented with a series of pictures, individually rated in terms of personal relevance (i.e., high versus low positive/negative emotional evocativeness) and categorized as social or non-social. Additionally, participants could prolong (approach) or shorten (avoid) the viewing-time of each picture, providing a measure of behavioral approach-avoidance. Intranasal OT enhanced both behavioral and neural approach (increased viewing-time), particularly towards negatively valenced pictures of both social and non-social nature, thus challenging the notion that OT’s effects are specific to social stimuli. Neurally, OT specifically amplified approach-related motivational salience of stimuli that were self-rated to have high personal relevance, but irrespective of their social nature or rated affective valence (positive/negative). Together, these findings provide support to the General Approach-Avoidance Hypothesis of OT, suggesting a role of OT in amplifying the motivational salience of environmental stimuli with high (personal) relevance, but irrespective of their social/non-social nature.Clinical Trial Number: The study design was registered at ClinicalTrials.gov (NCT04443647; 23/06/2020; https://clinicaltrials.gov/ct2/show/NCT04443647).

Highlights

  • Oxytocin (OT) plays a pivotal role in a variety of complex social behaviors by modulating approachavoidance motivational tendencies, but recently, its social specificity has been challenged

  • Related to its implicated role in promoting ‘pro-social’ behavior, intranasal administration of OT is increasingly considered as a potential treatment for a variety of neuropsychiatric disorders characterized by difficulties in the social domain, such as autism spectrum disorder (ASD)

  • In order to account for several observations of non-social effect of OT, such as OT-induced reduction of stress in non-social tasks in ­rodents[6] or increased eye gaze towards both social and non-social stimuli in h­ umans[7], the social approach/avoidance account was further elaborated into the General Approach-Avoidance Hypothesis of OT (GAAO;8)

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Summary

Introduction

Oxytocin (OT) plays a pivotal role in a variety of complex social behaviors by modulating approachavoidance motivational tendencies, but recently, its social specificity has been challenged. Intranasal OT enhanced both behavioral and neural approach (increased viewingtime), towards negatively valenced pictures of both social and non-social nature, challenging the notion that OT’s effects are specific to social stimuli. OT amplified approach-related motivational salience of stimuli that were self-rated to have high personal relevance, but irrespective of their social nature or rated affective valence (positive/negative). Together, these findings provide support to the General Approach-Avoidance Hypothesis of OT, suggesting a role of OT in amplifying the motivational salience of environmental stimuli with high (personal) relevance, but irrespective of their social/non-social nature. Among participants for whom negative emotion (anxious arousal) is motivationally-relevant, OT was shown to reduce behavioral avoidance of both social and non-social negatively valenced stimuli, providing important evidence that modulations of avoidance-related tendencies by OT are not limited to emotionally-evocative social stimuli, but extend to non-social stimuli as well

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